Duplicated antibiotic resistance genes reveal ongoing selection and horizontal gene transfer in bacteria

Duplicated antibiotic resistance genes reveal ongoing selection and horizontal gene transfer in bacteria

Horizontal gene transfer (HGT) and gene duplication are often considered as separate mechanisms driving the evolution of new functions. However, the mobile genetic elements (MGEs) implicated in HGT can copy themselves, so positive selection on MGEs could drive gene duplications. Here, we use a combi...

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Published in:Nature communications Vol. 15; no. 1; p. 1449
Main Authors: Maddamsetti, Rohan, Yao, Yi, Wang, Teng, Gao, Junheng, Huang, Vincent T., Hamrick, Grayson S., Son, Hye-In, You, Lingchong
Format: Journal Article
Language:English
Published: London Nature Publishing Group UK 16-02-2024
Nature Publishing Group
Nature Portfolio
Subjects:
38/23
631/158/855
631/181/2475
631/208/325/1506
631/326/22/1434
Antibiotic resistance
Antibiotics
Bacteria
Clinical isolates
Drug resistance
Enrichment
Evolution
Evolutionary genetics
Gene duplication
Gene sequencing
Gene transfer
Genes
Genomes
Horizontal transfer
Humanities and Social Sciences
Livestock
Microbial activity
Microorganisms
Modelling
multidisciplinary
Positive selection
Science
Science (multidisciplinary)
Transposition
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Summary:Horizontal gene transfer (HGT) and gene duplication are often considered as separate mechanisms driving the evolution of new functions. However, the mobile genetic elements (MGEs) implicated in HGT can copy themselves, so positive selection on MGEs could drive gene duplications. Here, we use a combination of modeling and experimental evolution to examine this hypothesis and use long-read genome sequences of tens of thousands of bacterial isolates to examine its generality in nature. Modeling and experiments show that antibiotic selection can drive the evolution of duplicated antibiotic resistance genes (ARGs) through MGE transposition. A key implication is that duplicated ARGs should be enriched in environments associated with antibiotic use. To test this, we examined the distribution of duplicated ARGs in 18,938 complete bacterial genomes with ecological metadata. Duplicated ARGs are highly enriched in bacteria isolated from humans and livestock. Duplicated ARGs are further enriched in an independent set of 321 antibiotic-resistant clinical isolates. Our findings indicate that duplicated genes often encode functions undergoing positive selection and horizontal gene transfer in microbial communities. Mobile genetic elements can promote the duplication of antibiotic resistance genes which may in turn accelerate the evolution of resistance to new drugs. Here, the authors show that duplicated antibiotic resistance genes are enriched in bacterial isolates from environments associated with rampant antibiotic use.
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ISSN:2041-1723
2041-1723
DOI:10.1038/s41467-024-45638-9